Biological Conservation 102 (2001) 1–16 www.elsevier.com/locate/biocon

Bird community structure along a trekking corridor of Himalaya: a conservation perspective

N. Chettria, E. Sharmaa,*, D.C. Debb aG. B. Pant Institute of Himalayan Environment and Development, Sikkim Unit, PO Tadong, Sikkim, 737102 bDepartment of Zoology, North Bengal University, Raja Rammohanpur, Darjeeling, India

Received 20 April 2000; received in revised form 10 February 2001; accepted 9 March 2001

Abstract community structure was studied in the Yuksam–Dzongri trekking corridor of the Sikkim Himalaya, India. Nineteen transects with a total of 266 samplings were made in the forests along the corridor during June 1997 to June 1999. Human utilised forest (open canopy forest) and relatively unutilised forest (closed canopy forest) were designated for the study at two ecological zones, i.e. lower forest (1780–2350 m a.s.l.) and upper forest (2350–3600 m) depending on the natural resources utilisation pattern by local community living in the area and for tourism purposes. There were visible changes in the open and closed canopy forests in diameters at breast height class distribution of trees leading to distinct variation in the habitat types. Among the 143 of observed during the study, a handful of species were found as habitat specific and about 40% were common to all the four habitat types. Both bird species richness and diversity were higher at the open canopy conditions compared with closed canopy, but the differences were not statistically significant. On the other hand, both the indices showed strong and significant negative relationship with the elevation. These diversity indices were also significantly higher during the summer compared with the winter season. The open canopy conditions exhibited comparatively more species of birds that were perturbated by human settlements than those species found at the closed canopy (mostly forest interior) and vice versa. Though the study could not trace out the effect of patch size brought about by human caused disturbances, the Yuksam–Dzongri trekking corridor possesses diverse habitat types as well as bird species resulted from heterogeneous habitat conditions. It is therefore important to emphasise disturbance study for threshold level assessment so that generalists as well as forest interior species could be managed through conservation efforts. # 2001 Elsevier Science Ltd. All rights reserved. Keywords: Forest types; Species richness and diversity; Habitat conditions; Seasonality

1. Introduction Javed, 1996; Safiq et al., 1997). Large scale habitat changes are occurring globally for fulfilling human Bird community evaluation has become an important needs that have caused habitat destruction, fragmenta- tool in biodiversity conservation and for identifying tion and degradation, necessiting assessment on the conservation actions in areas of high human pressure impacts of such change on birds (Brash, 1987; Whitten (Kremen, 1992; Safiq et al., 1997). Indian subcontinent et al., 1987; Khan et al., 1993). Determinations of bird is known for diverse and rich bird species whose tax- population in different habitats are central to under- onomy, distribution and their general habitat char- standing the community structure and niche relation- acteristics are well documented in India (Jerdon, 1862– ships, as well as for intelligent management of 1964; Bates and Lowther, 1952; Ali and Ripley, 1983). populations. Moreover seasonal monitoring is equally However, only a very little is known about bird com- important to trace the dynamic movement of birds in munity structure and their dynamics in India (Daniels, such habitats (Green and Catterall, 1998). 1989; Khan et al., 1993; Johnsingh and Joshua, 1994; The Eastern Himalaya (Khangchendzonga region) supports a wide diversity of birds resulting from complex physiography and bioclimatic zonation (Ives and Mes- * Corresponding author. Tel./fax: +91-3592-31090. serli, 1989) and also because of their location at the con- E-mail address: [email protected] (E. Sharma). vergence of the Palaearctic and Oriental Zoogeographical

0006-3207/01/$ - see front matter # 2001 Elsevier Science Ltd. All rights reserved. PII: S0006-3207(01)00092-1 2 N. Chettri et al. / Biological Conservation 102 (2001) 1–16

Realms (Inskipp, 1989). The area has been identified by issues of common interest for management (Sharma, the Birdlife International as a Priority I Endemic Bird 1997). Yuksam–Dzongri trekking corridor (26 km long) Area since it supports 25 restricted range bird species, of encompasses elevation from 1780 to 4000 m (Fig. 1). which 21 are confined to the region (Bibby, 1992). The trail passes through Sachen, Bakhim and Tshoka in Among eight species which were considered to be at risk the south-western part of Khangchendzonga Biosphere and listed as rare, vulnerable or endangered in the Reserve in Sikkim, India. Yuksam is a trailhead for this region (Carpenter, 1996), four species (satyra tragopan, corridor and leads to the Base Camp, Dzongri, cutia, short billed minivet and little pied fly- Thangsing and Gocha La in the West Sikkim (Fig. 1). catcher) have been recorded in the present study area Yuksam (1780 m) has 11 settlements with 274 house- (Chettri, 2000). holds comprising of 1573 people. One settlement with Bird studies in Sikkim date back to the 19th century eight households is inside the biosphere reserve at and many accounts on birds of Sikkim are available Tshoka (3000 m) on the trail. The majority of the ethnic (Bulger, 1869; Blandford, 1872; Gammie, 1877; Brooks, people of Yuksam are Subbas, followed by Bhutias, 1880; Ludlow and Kinnear, 1937, 1944; Mills, 1944; Lepchas, Nepalis and Tibetan Refugees mostly at Maclaren, 1947, 1948; Sen, 1948, 1957). Ali’s (1989) Tshoka. The primary occupation of the people is farm- ornithological work in the region is the most exhaustive ing while some are associated with tourism in the form to date. However, only a few more recent survey reports of lodge operators, porters, yakmen, cooks and guides are available. Some recent works have added about for trekking. Firewood and fodder collection, interior 30+ species to the list (Ganguli-Lachungpa, 1998). forest grazing and leaf litter collection are common Although bird , distribution and their general practices among the different ethnic groups. Tourism is habitats have been documented, there have been no increasing in the area at a rapid rate (Rai and Sundriyal, attempts for bird community study in Sikkim. 1997) and more people are engaged in this profession. Yuksam–Dzongri trekking corridor in west Sikkim is Annually, about 2000 domestic and foreign tourists visit an important tourist destination with great potential for the area. More than 150 support staff, 140 dzos (cross of bird watching. Disturbances such as firewood extrac- cow and yak) and 12 horses (pack ) operate in tion, fodder lopping and cattle grazing are worldwide this trekking trail on an average of six times a year. The problem and have increased during the last two decades Himalayan Mountaineering Institute (HMI) conducts in this trekking corridor due to growth in tourism and training for about 500 trainees annually in the area. population. These have resulted in the fragmentation Trekking tour staff including porters hired by travel and deterioration of wildlife habitats and also affecting agents and HMI trainees collect firewood for cooking the natural beauty of the area. Vegetation structure and heating purposes all along the corridor. This has showed remarkable changes in species composition at been one of the major factors of the forest destruction. human disturbed locations compared with relatively Four sampling stands were selected along the Yuksam– undisturbed areas along the corridor (Chettri, 2000). Dzongri trekking corridor (Fig. 1). Dominant trees and This could have major negative impacts on wildlife. An selective important species of all stand types are presented exploratory monitoring of birds in the area that in Table 1. Out of these four stands, two were located at encompassed a wide range of altitude and diverse forest warm temperate broadleaf forest having an elevation types is of special importance because of disturbances range 1780–2350 m and we designated the area as lower along the trek in recent years. This work would be use- forest (LF). Settlements around Yuksam generally ful for comparison in the follow-up study after a few depend on this forest for firewood, fodder and timber. more years of tourism in the area. The paper is an The other two stands were located at cool-temperate attempt to assess (1) bird diversity, (2) species composi- and sub-alpine zone having an elevation range 2350– tion and abundance and (3) seasonal variation on bird 3600 m, were designated as upper forest (UF). Settle- community structure at highly disturbed and relatively ment from Tshoka and tourism depend on this forest. undisturbed forests along the Yuksam–Dzongri trek- king corridor of west Sikkim. The study provides infor- 2.1. Vegetation surveys mation on effects on bird community in relation to habitat management implications. A total of 19 permanent plots measuring 3040 m were laid along the trekking corridor. The plots rela- tively undisturbed and distant from the settlement with 2. Methods >40% canopy cover, were designated as closed canopy forest (CC), while the plots extensively disturbed located The Khangchendzonga area is a unique mountain near the human settlement with <40% canopy cover, ecosystem falling in three different national boundaries were designated as open canopy forest (OC). Trees in of India, Nepal and Tibetan Autonomous Region of the the permanent plots were identified and their diameters People’s Republic of and has many transboundary at breast height (dbh) were measured using diameter N. Chettri et al. / Biological Conservation 102 (2001) 1–16 3

Fig. 1. Location map showing the Yuksam–Dzongri trekking corridor in west Sikkim. 4 N. Chettri et al. / Biological Conservation 102 (2001) 1–16 tape. Trees were separated into 10 dbh classes, and efficiency (Burnham et al., 1980) and ease of sampling density of each dbh class was compared between CC compared with other methods (Verner, 1985; Javed, and OC. Tree height was measured using a clinometer. 1996). The enlisted species were catagorised into differ- Nine height classes of trees (1–5, 6–10, 10–15, 16–20, 21– ent guilds depending on their feeding habit and the 25, 26–30, 31–35, 36–40 and >40 m) and their abun- migratory pattern following information gathered from dance were recorded in the four stands that were used existing literature and personal observations (Ali, 1989). for drawing tree height profile following Sankar Raman All the species that are common near the human settle- (1995) and Javed (1996) with necessary modifications. ments were considered as generalist species, and the species that were restricted to the forest interior were 2.2. Bird surveys considered as forest interior species (Ali and Ripley, 1983). Frequency of occurrence was used to identify The bird counts were conducted in 19 transects each species that were restricted to specific habitat in closed measuring 10040 m crossing each of the permanent canopy and open canopy conditions in the LF and UF plots (four each at closed canopy stand of LF and UF, following Hagan et al. (1997). Species diversity (Shan- five at open canopy stands at LF, and six at UF) during non–Wiener’s index), richness (Margalef species rich- summer (May–August) and during winter (October– ness) and Simpson index of dominance (Simpson index) February) following Hawrot and Niemi (1996), with were estimated in each transect following Hayek and necessary modifications. Three observations were made Buzas (1997). at each transect in a season during 1997–1998 (year 1) and 1998–1999 (year 2). Total numbers of transects 2.3. Data analysis surveyed were 266 (56 each in closed canopy stand of LF and UF, 70 in open canopy stand of LF, and 84 at Abundance of bird species was estimated from the UF). Bird surveys were made between 06:00–09:30 h in recorded number in each transect. The score was esti- the mornings, when wind was weak, to avoid tree mated as: branch movement for more accurate bird enumeration. Observations were not made during rainfall and foggy Pij ¼ mij=nj days to avoid bird visibility problem. During the sam- pling, all birds seen or heard in each transect were where mij is number of times recorded for species i and recorded and enlisted according to Oriental Bird Club’s nj is the total number of samples taken at site j. Differ- list (Inskipp et al., 1996). The Line Transect Method ences in the abundance between habitats for species was selected because of its robustness and sampling present at >3 transects were considered for GLM

Table 1 List of selective important species and dominant tree composition under closed and open canopy habitat conditions at the lower and upper forest types in the Yuksam–Dzongri trekking corridor

Forest type/elevation Habitat condition Tree domination Selective important species

Lower forest Closed canopy Quercus-Cinnamomum Quercus lamellosa, Cinnamomum impressinervium, 1780–2350 m Beilschmiedia sikkimensis, Quercus lineata, Eurya acuminata, Machilus edulis, Symplocos spp., Impatients, Elatostemma, etc.

Open canopy Quercus-Castanopsis Quercus lamellosa, Castanopsis spp., Eurya acuminata, Machilus edulis, Betula cylindrostachys, Viburnum cordifolia, Mahonia sikkimensis, Symplocos spp., Elatostemma sessile, Galinsuga, Polygonum, etc.

Upper forest Closed canopy Quercus-Acer, Abies-Rhododendron Acer papilio, Quercus lamellosa, Abies densa, 2350-3600 m Rhododendron falconeri, R. arboreum, R. grande, Magnolia campbelli, Impatients, Oxalis, Frageria, etc.

Open canopy Abies-Rhododendron Abies densa, Rhododendron arboreum, Magnolia campbelli, Prunus nepaulensis, Betula alnoides, Rosa sp., Frageria nubicola, Frageria sp., Viola, Porochetus, etc. N. Chettri et al. / Biological Conservation 102 (2001) 1–16 5

(general linear model). Effects of habitat conditions, 40% (57) were common among the four stands. Ninety- forest types and their interaction were analysed keeping eight species were present at >3 transects along the other attributes as random (Schutte and Niemi, 1998). corridor (Appendix). Grey-sided laughing thrush (9.90) Variations in species composition between the habitat was the most abundant species at the open canopy con- types were tested with replicated goodness of fit (G-test) dition of the LF followed by stripe-throated following Sokal and Rohlf (1981). (5.78) and grey-hooded warbler (4.12). In the closed Simple regressions were applied to examine diversity canopy condition, stripe-throated yuhina (6.32) was the trends with the elevations. Analysis of variance most abundant species followed by white-spectacled (ANOVA) was performed on density for variations warbler (5.50), (3.33) and buff-barred between year, seasons, forest types and habitat condi- warbler (3.25). Similarly, stripe-throated yuhina (6.00) tions. Seasonal changes in bird species diversity and was abundant at the closed canopy condition at UF richness were tested with a two-tailed t-test (Clergeau et followed by (4.00) and grey crested tit (3.80). In al., 1988). Some differences in count certainly could the open canopy condition, smokey warbler (3.92) was bring out variation on observations, as many species abundant followed by brown-headed tit babbler (3.67) were more easily detectable during specific time of the and grey-chinned minivet (3.61). year than the others (Best, 1981; Avery and Riper, Analysis of variance within GLM revealed that 22% 1989). These differences probably resulted from the dif- of species differed significantly between the two forest ference in seasonal behaviour (e.g. some species are types (LF and UF), 15% of species among the habitat more secretive while nesting) or environmental differ- conditions (CC and OC) and 20% of species as a result ences (CC provides more concealment than open of their interaction (forest types and habitat conditions). canopy). Adequate number of samplings have evaded Among the species showing significant differences the place for type I and type II errors (Block, 1989). All between habitat conditions (Appendix), white-throated statistical analyses were performed using SYSTAT, laughing thrush, grey-winged blackbird, grey-headed Version 6 (1996), unless otherwise mentioned. canary flycatcher, and black-faced laughing thrush were more abundant in the open canopy condition. On the other hand, rufous-bellied , white-tailed 3. Results nuthatch, Mrs Gould’s sunbird, and rufous-winged were more abundant in the 3.1. Vegetation closed canopy condition. There was a distinct partition on abundance of 32 species between the forest types (LF Density of dbh classes showed obvious differences in and UF). Among the noted species, grey-headed canary distribution at the CC and open canopy conditions of flycatcher, yellow napped yuhina, white-throated fan- both the LF and UF (Fig. 2). The distribution of dbh tail, verditor flycatcher, rufous-bellied niltava, blue classes was more regular in the closed canopy condition whistling thrush, white-throated laughing thrush, Mrs compared with the OC, indicating good regeneration Gould’s sunbird and grey-winged blackbird were more and representation of different size classes of trees. The abundant at the LF. Black-faced laughing thrush, plain- distribution pattern was skewed for the open condition backed thrush, spotted nutcracker, yellow-billed blue- at both the LF and UF suggesting disproportionate magpie, Eurasian tree-creeper and rufous-vented yuhina distribution of the tree sizes. were among the abundant species at the UF (Appen- Tree height profiles of the open canopy conditions dix). Large hawk cuckoo, grey-hooded warbler, rufous were remarkably disproportionate in their distribution sibia and verditor flycatcher differed significantly among different height classes compared with the closed between the forest types showing higher abundance at canopy condition (Fig. 3). Trees with 1–5 m height were the lower forest. Rufous bellied niltava, plain backed more abundant in the closed condition, whereas the thrush, green-tailed sunbird, blue whistling thrush, medium height trees were fewer at both the open and black-faced laughing thrush, Darjeeling , closed conditions in the lower forest. Small trees (1–5 m) white collared blackbird and grey winged blackbird were comparatively fewer at the UF suggesting poor were the species whose abundance varied significantly regeneration. Comparatively, 20–25 m height class trees between the habitat conditions as well as between the were less abundant at the UF compared with the LF. forest types (Appendix).

3.2. Bird species abundance 3.3. Habitat specificity

Over the 2-year period, 7149 bird detections (indivi- Of the 143 bird species, 10% of the species were duals) were made that represented 143 species during restricted to the CC in contrast with 16% in the OC of 266 visits distributed over 19 sampling transects placed LF (Fig. 4). At the CC of LF, the majority of species at four habitat stands. Of these 143 detected species, showed low frequency except the sultan tit (1.18) and 6 N. Chettri et al. / Biological Conservation 102 (2001) 1–16 grey-sided bush-warbler (1.18). The scenario at the OC breasted accentor, red-fronted rosefinch and black- of LF was also similar with few exceptions such as red- throated sunbird showed higher frequency. vented bulbul (2.39), little forktail (1.30), grey treepie (1.52) and black bulbul (1.30). At the UF, only 3% of 3.4. Bird community the total species were observed as unique for the CC. Spotted bush-warbler (1.57) and grandala (1.57) were Bird species diversity and richness were higher at both among the species with comparatively higher frequency. the forests in the open canopy condition (Table 2). Similarly at the OC, 6% of the total species was recor- Density of birds was also higher at the open canopy ded as specific to the habitat. Among them, rufous- condition of LF (30Æ2.3 per transect) compared with

Fig. 2. Diameter class distribution of tree density in closed and open canopy conditions at (a) the lower forest and (b) the upper forest along the Yuksam–Dzongri trail. dbh classes (cm) I=10–20, II=20–30, III=30–40, IV=40–50, V=50–60, VI=60–70, VII=70–80, VIII=80–90, IX=90– 100 and X=>100. N. Chettri et al. / Biological Conservation 102 (2001) 1–16 7

Table 2 Sample size, composition and structure of bird communities in different habitat conditions at the Yuksam–Dzongri trekking corridor

Bird variables Lower foresta Upper foresta

CC OC CC OC

Sampling size (100 m transect) 56 70 56 84 Species recorded 82 86 64 77 Species per transect (meanÆS.E.) 7Æ0.53 8Æ0.44 6Æ0.43 5Æ0.32 Individuals per transect (meanÆS.E.) 28Æ2.7 30Æ2.4 27Æ3.5 24Æ1.9 Shannon Weiner’s diversity (H0) 3.65 3.72 3.52 3.69 Margalef’s species richness index 10.3 11.2 8.7 10.1 Pielou’s eveness index 0.83 0.84 0.85 0.85 Simpson index of dominance 0.045 0.040 0.049 0.036

a CC, closed canopy condition; OC, open canopy condition.

Fig. 3. Foliage height abundance in two forest types showing well-stratified forest at closed canopy compared with open canopy at the Yuksam– Dzongri trekking corridor. (a=lower forest, open canopy; b=lower forest, closed canopy; c=upper forest, open canopy and d=upper forest, closed canopy). 8 N. Chettri et al. / Biological Conservation 102 (2001) 1–16 that of the closed canopy (28Æ2.7 per transect), and the Species composition (number of species per transect) values were reversed at UF (24Æ1.9 per transect) at the varied significantly between the year (F1,246=8.5, open canopy compared with the closed canopy condi- P=0.004), season (F1,246=7.04, P=0.008) and forest tion (27Æ3.5 per transect). Mann–Whitney U test of type (F1,246=21.1, P=0.0001). Interactions between the species richness, diversity, density, and bird abundance year and season only (F1,246=8.1, P=0.005, did not show any significant variation between the LSD0.05=2.29) were found to be significant (Fig. 5). habitat conditions. In contrast, all these variables were However, density of bird showed strong interaction significantly different between the two-forest types between the year and season (F1,246=16.1, P=0.0001), (Table 3). Considerable dissimilarities in species assem- year and habitat condition (F1,246=5.9, P=0.016), sea- blages exist between the two habitat conditions. Species son and forest type (F1,246=3.8, P=0.056) and habitat assemblages differed significantly among the habitat condition, year and forest type (F1,246=6.6, P=0.011, conditions at the lower forest (G=174, P=<0.01) and LSD0.05=14.14; Fig. 6). Bird species richness and upper forest (G=595.32, P=<0.01), and the difference diversity, and tree species richness and diversity showed was more pronounced (G=2738, P=<0.001) between strong negative and linear trend with increasing eleva- the two forest types (lower and upper forests). tions. The relationships for bird species richness and

Table 3 Comparative assessment of bird community structure between habitat (closed canopy and open canopy) and forests (lower forest and upper forest) of the Yuksam–Dzongri trekking corridor

Variable Effect of habitat condition Effect of forest types

Mann–Whitney U-valuea X2c P Mann–Whitneyb U-value X2b P

Bird species richness 8788.0 0.61 0.43 CCOC Density 8461.0 0.06 0.81 CCOC

a U 0.05(2),154,108 b U 0.05(2),122,140. c Chi-square approximation with d.f. 1. d CC, closed canopy condition; OC, open canopy condition.

Fig. 4. Bird species with frequency observed at specific habitat types at the Yuksam–Dzongri trekking trail. (LF=lower forest, UF=upper forest, OC=open canopy, CC=closed canopy). N. Chettri et al. / Biological Conservation 102 (2001) 1–16 9 diversity were stronger with increasing elevation than d.f.=82, P=0.003) showed a strong variation in bird tree species richness and diversity (Fig. 7). species diversity.

3.5. Seasonal variation of bird community 4. Discussion

The bird species richness and diversity varied sig- The Yuksam–Dzongi trekking corridor forest is nificantly between the summer and winter seasons at all highly diverse both in and birds. Tree dbh class the habitats except at the closed canopy of UF (Table 4). density and height class abundance revealed that the The open canopy conditions at both the forest types open forests have a disproportionate distribution of (LF-t=2.50, d.f.=68, P=0.016, and UF-t=3.05, trees in the areas with human disturbances, suggesting

Fig. 5. Bird species composition in breeding and non-breeding seasons for two years (Year 1=1997–1998, Year 2=1988–1999) in the open and closed canopy conditions of the lower and upper forests in the Yuksam–Dzongri trekking corridor. ANOVA: Year F1,246=8.5, P<0.004; Season F1,246=7.04, P<0.008; Forest type F1,246=21.1, P<0.0001, YearSeason F1,246=8.1, P< 0.005; other interaction not significant, LSD(0.05)=2.29. (LF=lower forest, UF=upper forest, OC=open canopy, CC=closed canopy).

Fig. 6. Bird density in breeding and nonbreeding seasons for two years (Year 1=1997–1998, Year 2=1988–1999) in the open and closed conditions of the lower and upper forests in the Yuksam–Dzongri trekking corridor. ANOVA: Variations due to year, seasons and forest types were significant;

YearSeason F1,246=16.1, P<0.0001; Yearforest type condition F1,246=5.9, P<0.016; SeasonForest type F1,246=3.8, P<0.056, YearSeasonYearForest type F1,246=6.6, P< 0.011; other interaction not significant, LSD(0.05)=14.14 (LF=lower forest, UF=upper forest, OC=open canopy, CC=closed canopy). 10 N. Chettri et al. / Biological Conservation 102 (2001) 1–16

Table 4 Comparison of bird species richness (BSR) and bird species diversity (BSD) between summer (S) and winter (W) seasons in the Yuksam–Dzongri trekking corridor

Forest type Habitat condition Bird variables t-statistica d.f.

Lower forest Closed canopy BSR t=2.50 P=0.016* 50 S>W S.E.=0.75 CI (0.049–1.354) BSD t=2.65 P=0.011* 50 S>W S.E.=0.49 CI (0.117–0.879) Open canopy BSR t=2.31 P=0.024* 68 S>W S.E.=0.53 CI (0.072–0.992) BSD t=2.70 P=0.009** 68 S>W S.E.=0.39 CI (0.102–0.681)

Upper forest Closed canopy BSR t=0.686 P=0.780 54 S>W S.E.=0.22 CI (0.4250–0.867) BSD t=1.78 P=0.081 54 S>W S.E.=0.32 CI (0.042–0.696) Open canopy BSR t=3.42 P=0.001* 82 S>W S.E.=0.58 CI (0.245–0.927) BSD t=3.05 P=0.003** 82 S>W S.E.=0.39 CI (0.138–0.650)

a t-Test for pair samples. *P<0.05. **P<0.01.

Fig. 7. Relationship on woody tree species richness and diversity, and bird species richness and diversity with elevation in the forests (O=open canopy and C=closed canopy) of the Yuksam–Dznogri trekking corridor. Elevation transformed to natural log. N. Chettri et al. / Biological Conservation 102 (2001) 1–16 11 high pressure on lower dbh classes or smaller-height open canopy condition, near human settlements, in trees. Field observation revealed that regeneration of association with other forest species which is an indica- canopy trees is poor at the disturbed stands due to tion of disturbances (Restrepo and Gomez, 1998). This grazing and trampling, which were comparatively more has suggested that they are habitat generalists that tend abundant at the undisturbed stands (Chettri, 2000). to be less sensitive to habitat changes than the forest However, abundance of 1–5 m class trees at open interior birds (Telleria and Santos, 1995). The open canopy in the upper forest was relatively higher. This condition, where secondary tree species (Symplocos could be due to lower levels of firewood extraction ramisissima, Viburnum cordifolia and Mahonia sikki- because of low human pressure resulting in better mensis) are dominant, showed fewer forest birds with regeneration. Lower abundance of medium height trees more of the generalist species than in the closed canopy, (11–20 m) at the open canopy and even at the closed supporting a similar observation by Beehler et al. (1987) canopy stands of the lower forest attributed preference and Terborgh and Weske (1969). Many interior forest for extraction of moderate sized trees as firewood by the dwelling birds, such as chestnut-tailed minla, white- local people. The pressure is higher at the LF which is in spectacled warbler, buff-barred warbler, greenish war- the vicinity of Yuksam settlement with a larger popula- bler and little-pied flycatcher, have higher abundance at tion residing here. the closed canopy condition where the structural com- The vegetation structure suggests that human pres- plexity like vertical stratification with higher canopy sure has reduced the quality of the species composition coverage is maintained than at the open canopy condi- in the open canopy forest providing accessible foraging tion. Fremark and Collins (1992) have also reported ground for different bird species. Bird density was similar results for forest birds at habitat with greater higher at the open canopy condition in the LF. This is overall forest cover than at the open areas. These results obvious that an opening of canopy creates more ground support that the open and closed canopy forest pos- for resources and all general species as well as species sesses wide structural pattern in context of forest strati- that are adjustable to such condition, will exploit the fication, which in turn provides habitat for breeding and area (Block, 1989; Daniels, 1989). In the present study, feeding ground to the species as per their habitat pre- the density has not been used for interpretation of ferences (Verner and Larson, 1989; Javed, 1996; Shafiq habitat quality as the results may be misleading unless et al., 1997). A significant seasonal change of bird spe- other attributes are considered (Van Horne, 1983; cies diversity and richness at different habitat types Vickery et al., 1992). Bird species richness as well as suggests that the bird species of this corridor have diversity were higher at the open canopy conditions of dynamic seasonal movement including that of long dis- the LF, but were not significantly different between the tance migrants (white capped-water redstart, Rufous- two conditions. Comparatively, insignificantly higher bellied niltava, stripe-throated yuhina, etc.). This is bird species richness at the open condition of lower for- apparent as about 40% of the total recorded species est could be due to a pattern consistent with the edge were common in all the four stands and the majority effect (Kilgo et al., 1997). Fleming and Giuliano (1998) being local migrants. Seasonal movements of species for from their experimental work in border-edge cut and food searching might have brought about such fluctua- uncut plots, suggested that the species richness does not tions. There might be other factors unrelated to habitat differ significantly among the plots due to similar rea- disturbances that contributed to the difference in bird sons. Daniels (1989) also reported similar results that assemblages between the closed and open canopy con- supported the findings. The reason could be that the ditions. The principal differences among these sites were present study plots were undoubtedly smaller than the undoubtedly due to human pressure resulting in chan- individual home ranges and probably that the plots ges in vegetation structure and composition (Block and were used by individuals relying on suitable habitat of Morrison, 1991; Block and Brennan, 1993; Aigner et al., surrounding forests (Aigner et al., 1998), or size of pat- 1998). To maintain the bird community, further degra- ches (open forest area) formed were small enough to dation of the habitat has to be minimised by regulating bring about variation in bird species diversity (Kilgo et human activities (Johnsingh and Joshua, 1994). al., 1998). Significant differences in species assemblages between the open and closed canopy conditions could be 5. Conclusion explained by the fact that many common species have dominance on the open canopy in association with some It is apparent from the earlier discussions that the forest birds (MacArthur, 1972). Generalists or common Yuksam–Dzongri trekking corridor exhibits diverse species, e.g. like black drongo, red-vented bulbul, grey habitat types, rich in bird species. A wide range of bushchat, green-backed tit including lemmon-rumped habitat types are available for birds that are equally uti- warbler, grey-headed canary flycatcher warbler, verditor lised. Only a handful of bird species have restricted them- flycatcher and house crow, were more abundant at the selves to specific habitats, either to the open canopy or 12 N. Chettri et al. / Biological Conservation 102 (2001) 1–16 closed canopy conditions in the lower and upper forests. and timber extractions and grazing, brought about sub- This reflects that the majority of birds use a variety of tle changes in available habitats for birds. It appears available habitats over their entire geographical range. apparent that birds represent habitat not only by dis- The presence of a wide variety of species such as wood- turbance level but resource availability is another peckers, flycatchers, tits, drongos and warblers indicates important factor for maintenance which needs to be the richness of woodland birds in the area. Though kept in mind for bird conservation initiatives. A detailed there are distinct differences in the vegetation structure study on effects of patch size created by disturbances between the open and closed canopy conditions, differ- and surrounding habitat is necessary to come to any ences in bird diversity are not statistically significant. conclusive interpretation. The high human pressure at Bird species richness and density showed strong inter- the lower forest may lead to greater patch formation action with temporal as well as ecological complexities and edge extension in the long term, which have more of forests but not with the habitat conditions. However, impact on birds than species composition. Many the individual species and species assemblage responses environmental awareness programmes were conducted to their habitats are more convincing. This suggests that for the community and tourism enterprises by the Sik- individual response and species assemblages to the kim Biodiversity and Ecotourism Project; however, available habitats provide better interpretation on more effective measures are required for minimising habitat use than the diversity indices. human pressure on the natural resources of the area. The open canopy conditions in both forest types Extensive and long-term studies are also necessary to showed more generalist species and higher diversity, evaluate the importance of site fidelity in obscuring which is an indication of disturbances and is substantiated effects in the short term and to describe the persistence by poor diversity at the closed canopy condition. Our of the effect. observation implies that the human disturbances at the open canopy forest might have brought about visible change in forest birds, providing a more open understorey for generalist species as observed in the lower forest. On Acknowledgements the other hand, with negligible change in vegetation complexity at the upper forest, the differences in bird The authors are thankful to the Director, G. B. Pant community was due less to low human interference. This Institute of Himalayan Environment and Development, condition has shown less effect on bird species diversity. and The Mountain Institute, USA for facilities. This It is apparent from the aforementioned discussion that research was supported under Sikkim Biodiversity and small-scale variation in diversity could be due to seaso- Ecotourism Project, which received a grant from the nal migratory patterns of species looking for resources. Biodiversity Conservation Network funded by USAID. Thus, our short-term (2-year) observation could not IDRC-Canada also provided financial support to Nakul trace out clearly the possible reason for such changes. Chettri. Dr. Ajith Kumar of Salim Ali Center for Wild- The study revealed that the forest interior species and life and Ornithology, Coimbatore, critically reviewed general species have distinctness in their habitat use. the manuscript. Small-scale human pressures such as firewood, fodder

Appendix. Bird species abundance on 98 species that were encountered in >3 transects and the result on ANOVA within GLM between two forest types and two habitat conditions from the Yuksam–Dzongri trekking trail, West Sikkim. Codea Common name (Latin name) Lower forestb Upper forest FTHCc HC FT CC OC CC OC PPP 64 Blood Pheasant (Ithaginis cruentus) – – 3.44 0.92 0.02 0.03 0.04 209 Darjeeling Woodpecker ( darjellensis) 0.18 0.07 0.86 0.71 <0.01 <0.01 <0.01 226 Golden-throated Barbet (Megalaima franklinii) – 0.53 – – 0.01 0.08 0.03 267 Great Barbet (Megalaima virens) 0.23 0.24 – – <0.01 0.02 <0.01 309 Eurasian Hoopoe (Upupa epops) – – 0.25 – 0.25 0.25 0.35 380 Large Hawk Cuckoo (Cuculus sparverioides) – 0.55 0.06 – <0.01 0.02 <0.01 384 Indian Cuckoo (Cuculus micropterus) 0.25 0.16 – – 0.02 0.03 0.01 633 Snow Pigeon (Columba leuconata) – – – 2.25 0.36 0.32 0.26 1050 Common Kestrel (Falco tinnunculus) 0.25 – – – 0.25 0.25 0.31 (Continued on next page) N. Chettri et al. / Biological Conservation 102 (2001) 1–16 13

Appendix (continued) Codea Common name (Latin name) Lower forestb Upper forest FTHCc HC FT CC OC CC OC PPP 1302 Yellow-billed Blue Magpie (Urocissa flavirostris) 0.17 0.25 0.96 2.03 <0.01 <0.01 <0.01 1310 Grey Treepie (Dendrocitta formosae) – 1.24 – – 0.09 0.17 0.09 1314 Collared Treepie (Dendrocitta frontalis) – 2.60 – – 0.04 0.12 0.05 1323 Spotted Nutcraker (Nucifraga caryocatactes) – – 0.60 0.43 <0.01 <0.01 <0.01 1328 House Crow (Corvus splendens) – 1.30 – – 0.27 0.33 0.22 1333 Long-billed Crow (Corvus macrorhynchos) – – 0.73 1.18 0.01 0.03 <0.01 1340 Common Raven (Corvus corax) 0.17 – 0.17 0.39 0.08 0.06 0.06 1411 Grey-chinned Minivet (Pericrocotus solaris) – 2.00 – 3.61 0.11 0.09 0.07 1413 Short-billed Minivet (Pricrocotus brevirostris) 0.50 1.10 0.38 0.71 0.06 0.04 0.03 1415 Scarlet Minivet (Pricrocotus flammeus) 1.44 1.10 – – <0.01 0.02 <0.01 1418 Yellow-bellied Fantail (Rhiphidura hypoxantha) 0.83 0.80 – 0.22 0.08 0.09 0.06 1423 White-throated Fantail (Rhiphidura albicollis) 0.98 0.75 – 0.09 <0.01 <0.01 <0.01 1437 Black Drongo (Dicrurtus adsimilis) 0.29 0.77 – – 0.02 0.06 0.01 1485 Blue Rock Thrush (Monticola solitarius) 0.28 0.64 0.22 0.37 0.02 0.01 <0.01 1491 Bluewhisling Thrush (Myiophonus caeruleus) 0.59 0.49 0.07 0.05 <0.01 <0.01 <0.01 1507 Plain-backed Thrush (Zoothera mollissima) 0.09 0.09 0.39 0.61 <0.01 <0.01 <0.01 1512 Long-billed Thrush (Zoothera monticola) 0.08 0.47 0.58 0.67 0.01 0.01 <0.01 1513 Dark-sided Thrush (Zoothera marginata) 0.25 0.40 – 0.17 0.14 0.14 0.09 1517 Rufous-gorgetted Flycatcher (Musicapa strophiata) 0.56 0.90 0.63 0.13 0.02 0.02 0.02 1520 White-collared Blackbird (Turdus albocintus) 0.20 0.08 0.35 0.63 <0.01 <0.01 <0.01 1521 Grey-winged Blackbird (Turdus boulboul) 0.44 0.08 0.28 0.38 <0.01 <0.01 <0.01 1586 Littlepied Flycatcher (Ficedula westermanni) 2.00 0.40 – – 0.04 0.06 0.06 1593 Verditor Flycatcher (Eumyias thalassina) 0.25 0.86 – 0.05 <0.01 <0.01 <0.01 1598 Large Niltava (Niltava grandis) 0.13 0.50 – – 0.17 0.21 0.13 1601 Rufous-bellied Niltava (Niltava sundara) 0.66 0.13 0.13 0.21 <0.01 <0.01 <0.01 1659 Daurean Redstart (Phoenicurus auroreus) – 0.60 – 0.29 0.05 0.05 0.03 1661 Blue-fronted Redstart (Phoenicurus frontalis) 0.33 0.47 – 0.11 0.04 0.05 0.03 1662 White-capped Water Redstart (Chaimarrornis 0.13 0.30 – 0.17 0.09 0.14 0.06 lecocephalus) 1663 Plumbus Water Redstart (Rhyacornis fuliginosus) – 0.40 – – 0.04 0.12 0.05 1669 Grandala (Grandala coelicolar) – – 0.75 – 0.08 0.11 0.2 1687 Grey Bushchat (Saxicola ferrea) – 1.35 – – 0.03 0.11 0.04 1743 White-tailed Nuthach (Sitta himalayansis) 0.57 0.18 0.52 0.23 <0.01 <0.01 <0.01 1756 Eurasian Tree-creeper (Certhia familaris) 0.06 0.05 0.34 0.31 <0.01 <0.01 <0.01 1764 Fire-capped Tit (Cephalopyrus flammiceps) – – 1.50 1.00 0.12 0.11 0.11 1771 Rufous-vented Tit (Parus rudeventris) 0.11 0.05 3.32 2.24 0.02 0.02 0.01 1773 Coal Tit (Parus ater) – – 4.00 0.67 0.07 0.08 0.12 1777 Grey-creasted Tit (Parus dichrous) – – 3.80 2.00 0.01 0.02 0.01 1780 Green-backed Tit (Parus monticolus) 0.08 1.73 – – 0.01 0.07 0.02 1793 Black-throated Tit (Aegithalos concinnus) 1.88 2.00 – – 0.05 0.08 0.03 1796 Black-browed Tit (Aegithalos iouschistos) – – 2.25 0.56 0.04 0.06 0.08 1817 Goldcrest (Regulus regulus) – – 2.50 1.17 0.08 0.08 0.09 1822 Straighted Bulbul (Pycnonotus straitus) 0.06 0.45 – – 0.11 0.17 0.09 1837 Red-vented Bulbul (Pycnonotus cafer) – 0.71 – – 0.04 0.13 0.05 1879 Black Bulbul (Hypsipetes leucocephalus) – 1.07 – – 0.02 0.09 0.04 2008 Smokey Warbler (Phylloscopus fuligiventer) – – 1.25 3.92 0.31 0.26 0.22 2009 Tickle’s Leaf Warbler (Phylloscopus affinis) 1.32 3.06 0.14 0.81 <0.01 0.02 <0.01 2014 Buff-barred Warbler (Phylloscopus pulcher) 3.25 0.60 – – 0.02 0.04 0.04 2017 Lemmon-rumped Warbler (Phylloscopus proregulus) 2.00 3.60 0.75 – 0.01 0.03 0.01 2023 Greenish Warbler (Phylloscopus trochiloides) 3.33 1.04 0.92 1.04 <0.01 <0.01 <0.01 2043 Golden-spectacled Warbler (Seicercus burkii) 0.25 0.20 – – 0.04 0.06 0.03 (Continued on next page) 14 N. Chettri et al. / Biological Conservation 102 (2001) 1–16

Appendix (continued) Codea Common name (Latin name) Lower forestb Upper forest FTHCc HC FT CC OC CC OC PPP 2044 Grey-hooded Warbler (Seicercus xanthoschitos) 3.65 4.12 1.05 – <0.01 <0.01 <0.01 2045 White-spectacled Warbler (Seicercus affinis) 5.50 3.60 2.00 1.33 0.02 0.02 0.01 2052 Black-faced Flycatcher-Warbler (Abroscopus schisticeps) 1.13 – 1.00 0.17 0.06 0.04 0.09 2053 Yellow-bellied Warbler (Abrocopus superciliaries) 2.00 3.60 – 0.75 0.85 0.06 0.06 2064 White-throated Laughing Trush (Garrulax albogularis) 0.88 0.73 1.33 0.67 <0.01 <0.01 <0.01 2069 Straighted Laughing Trush (Garrulax straitus) 0.80 1.36 – – <0.01 0.03 <0.01 2087 Spotted Laughing Thrush (Garrulax occellatus) 0.06 0.15 0.13 0.25 0.17 0.18 0.13 2088 Grey-sided Laughing Trush (Garrulax caerulatus) 0.50 9.90 2.00 0.33 <0.01 0.03 <0.01 2099 Blue-winged Laughing Trush (Garrulax sqamatus) 0.75 0.10 0.25 0.08 <0.01 <0.01 0.01 2104 Black-faced Laughing Trush (Garrulax affinis) 0.11 0.07 0.14 0.46 <0.01 <0.01 <0.01 2110 Red-faced Liocichla (Liocichla phoenicea) 0.25 0.30 – 0.08 0.07 0.07 0.04 2223 Redbilled Leiothrix (Leiothrix lutea) – 0.60 – 0.46 0.15 0.13 0.09 2226 White-browed Shrike-Babbler (Pteruthius flaviscapis) 0.33 – 0.17 – 0.03 0.03 0.08 2227 Green Shrike-Babbler (Pteruthius xanthoclorus) – 0.80 – – 0.37 0.41 0.31 2231 Rusty-fronted Barwing (Actinodura egertoni) 0.44 0.10 – – 0.01 0.03 0.03 2238 Chesnut-tailed Minla (Minla strigula) 0.19 – 1.00 – 0.02 0.02 0.09 2243 Chestnutheaded Tit-Babbler (Alcippe castaneceps) 1.42 1.20 0.58 0.30 <0.01 <0.01 <0.01 2244 White-browed Tit-Babbler (Alcippe vinipectus) 1.06 – 0.50 2.13 0.12 0.11 0.09 2247 Brownheaded Tit-Babbler (Alcippe cinereiceps) 0.50 – – 3.67 0.38 0.33 0.29 2261 Rufous Sibia (Heterophasia capistrata) 0.44 2.22 0.04 – <0.01 0.03 <0.01 2270 Whiskered Yuhina (Yuhina flavicollis) 2.41 2.28 0.13 0.48 <0.01 <0.01 <0.01 2272 Stripe-throated Yuhina (Yuhina gularis gularis) 6.32 5.78 6.00 3.83 0.33 <0.01 <0.01 2274 Rufous-vented Yuhina (Yuhina occipitalis) 0.13 – 2.66 2.42 <0.01 0.02 <0.01 2393 Mrs. Gould’s Sunbird (Aethopyga gouldiae) 0.75 0.70 0.38 0.58 <0.01 <0.01 <0.01 2394 Green-tailed Sunbird (Aethopyga nipalensis) 0.30 0.68 0.25 0.13 <0.01 <0.01 <0.01 2401 Firetailed Sunbird (Aethopyga ignicauda) 0.63 0.40 0.38 0.33 0.02 0.02 0.02 2410 Streaked Spiderhunter (Aracnothera magma) 0.50 1.00 – – 0.13 0.16 0.09 2413 House Sparrow (Parus domesticus) 1.00 – – 1.08 0.11 0.1 0.09 2416 Russet Sparrow (Passer rutilans) 1.25 0.60 – – 0.02 0.04 0.02 2438 Blyth’s Pipit (Anthus godlewskii) 0.13 0.03 0.22 1.94 0.12 0.11 0.07 2441 Olive-backed Pipit (Anthus hodgsoni) 0.25 – 1.00 1.42 0.09 0.08 0.07 2459 Marron-backed Accentor (Prunella immaculate) – – 0.83 0.61 0.09 0.09 0.08 2506 Black-headed Mountain-Finch (Leucosticte brandti) – – 0.21 0.52 0.09 0.09 0.06 2516 Dark-breasted Rosefinch (Carpodacus nipalensis) – – 0.50 1.06 0.14 0.12 0.09 2520 Pink-browed Rosefinch (Carpodacus rhodochorus) – – 0.50 0.39 0.05 0.06 0.04 2531 Redbreasted Rosefinch (Carpodacus puniceus) – – – 0.83 0.35 0.31 0.26 2542 Red-headed Bullfinch (Pyrrhula erythrocephala) – – 1.35 1.47 0.05 0.06 0.03 2549 Collared Grossbeak (Mycerobas affinis) – – 0.35 0.87 0.18 0.16 0.12 2551 White-winged Grossbeak (Mycerabas carnipes) – – 0.25 0.67 0.16 0.14 0.11

a OBC codes (Inskipp et al., 1996). b CC, closed canopy condition; OC, open canopy condition. c FT, forest types; HC, habitat conditions.

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